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2. The cold-induced factor CBF3 mediates root stem cell activity, regeneration, and developmental responses to cold

Author

Ministerio de Ciencia e Innovación (España), Agencia Estatal de Investigación (España), Comunidad de Madrid, Pucciariello, Ornella [0000-0002-5241-5385], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], Cabrera, Javier [0000-0002-9277-4876], del Barrio, Cristina [0000-0002-7829-2109], del Pozo, J. C. [0000-0002-4113-457X], Perales, Mariano [0000-0002-7351-8439], Wabnik, Krzysztof [0000-0001-7263-0560], Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], Pérez-García, Pablo, Pucciariello, Ornella, Sanchez-Corrionero, Alvaro, Cabrera, Javier, del Barrio, Cristina, del Pozo, J. C., Perales, Mariano, Wabnik, Krzysztof, Moreno-Risueño, Miguel Ángel, Ministerio de Ciencia e Innovación (España), Agencia Estatal de Investigación (España), Comunidad de Madrid, Pucciariello, Ornella [0000-0002-5241-5385], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], Cabrera, Javier [0000-0002-9277-4876], del Barrio, Cristina [0000-0002-7829-2109], del Pozo, J. C. [0000-0002-4113-457X], Perales, Mariano [0000-0002-7351-8439], Wabnik, Krzysztof [0000-0001-7263-0560], Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], Pérez-García, Pablo, Pucciariello, Ornella, Sanchez-Corrionero, Alvaro, Cabrera, Javier, del Barrio, Cristina, del Pozo, J. C., Perales, Mariano, Wabnik, Krzysztof, and Moreno-Risueño, Miguel Ángel

Abstract

Plant growth and development involve the specification and regeneration of stem cell niches (SCNs). Although plants are exposed to disparate environmental conditions, how environmental cues affect developmental programs and stem cells is not well understood. Root stem cells are accommodated in meristems in SCNs around the quiescent center (QC), which maintains their activity. Using a combination of genetics and confocal microscopy to trace morphological defects and correlate them with changes in gene expression and protein levels, we show that the cold-induced transcription factor (TF) C-REPEAT BINDING FACTOR 3 (CBF3), which has previously been associated with cold acclimation, regulates root development, stem cell activity, and regeneration. CBF3 is integrated into the SHORT-ROOT (SHR) regulatory network, forming a feedback loop that maintains SHR expression. CBF3 is primarily expressed in the root endodermis, whereas the CBF3 protein is localized to other meristematic tissues, including root SCNs. Complementation of cbf3-1 using a wild-type CBF3 gene and a CBF3 fusion with reduced mobility show that CBF3 movement capacity is required for SCN patterning and regulates root growth. Notably, cold induces CBF3, affecting QC activity. Furthermore, exposure to moderate cold around 10°C-12°C promotes root regeneration and QC respecification in a CBF3-dependent manner during the recuperation period. By contrast, CBF3 does not appear to regulate stem cell survival, which has been associated with recuperation from more acute cold (∼4°C). We propose a role for CBF3 in mediating the molecular interrelationships among the cold response, stem cell activity, and development.

Published
2023

4. Fine-tuned nitric oxide and hormone interface in plant root development and regeneration.

Author

Sanchez-Corrionero, Alvaro, Sánchez-Vicente, Inmaculada, Arteaga, Noelia, Manrique-Gil, Isabel, Gómez-Jiménez, Sara, Torres-Quezada, Isabel, Albertos, Pablo, and Lorenzo, Oscar

Subjects
*ROOT development, *PLANT development, *PLANT roots, *PLANT hormones, *STEM cell niches, *REGENERATION (Botany)
Abstract

Plant root growth and developmental capacities reside in a few stem cells of the root apical meristem (RAM). Maintenance of these stem cells requires regenerative divisions of the initial stem cell niche (SCN) cells, self-maintenance, and proliferative divisions of the daughter cells. This ensures sufficient cell diversity to guarantee the development of complex root tissues in the plant. Damage in the root during growth involves the formation of a new post-embryonic root, a process known as regeneration. Post-embryonic root development and organogenesis processes include primary root development and SCN maintenance, plant regeneration, and the development of adventitious and lateral roots. These developmental processes require a fine-tuned balance between cell proliferation and maintenance. An important regulator during root development and regeneration is the gasotransmitter nitric oxide (NO). In this review we have sought to compile how NO regulates cell rate proliferation, cell differentiation, and quiescence of SCNs, usually through interaction with phytohormones, or other molecular mechanisms involved in cellular redox homeostasis. NO exerts a role on molecular components of the auxin and cytokinin signaling pathways in primary roots that affects cell proliferation and maintenance of the RAM. During root regeneration, a peak of auxin and cytokinin triggers specific molecular programs. Moreover, NO participates in adventitious root formation through its interaction with players of the brassinosteroid and cytokinin signaling cascade. Lately, NO has been implicated in root regeneration under hypoxia conditions by regulating stem cell specification through phytoglobins. [ABSTRACT FROM AUTHOR]

Published
2023
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6. An auxin-regulable oscillatory circuit drives the root clock in Arabidopsis

Author

Ministerio de Economía y Competitividad (España), European Commission, Comunidad de Madrid, Research Foundation - Flanders, Agencia Estatal de Investigación (España), Ministerio de Ciencia e Innovación (España), Perianez-Rodriguez, Juan [0000-0003-1002-7111], Rodriguez, Marcos [0000-0003-3741-8593], Marconi, Marco [0000-0002-3457-1384], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Wachsman, Guy [0000-0002-0551-9333], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], De Gernier, Hugues [0000-0002-7644-3233], Cabrera, Javier [0000-0002-9277-4876], Perez-Garcia, Pablo [0000-0001-8595-8530], Gude, Inmaculada [0000-0002-3122-1688], Saez, Angela [0000-0002-9189-4737], Serrano-Ron, Laura [0000-0001-5180-6547], Beeckman, Tom [0000-0001-8656-2060], Benfey, Philip N [0000-0001-5302-758X], Rodríguez-Patón, Alfonso [0000-0001-7289-2114], del Pozo, J. C. [0000-0002-4113-457X], Wabnik, Krzysztof [0000-0001-7263-0560], Moreno-Risueno, Miguel A [0000-0002-9794-1450], Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, De Gernier, Hugues, Cabrera, Javier, Pérez-García, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N., Rodríguez-Patón, Alfonso, del Pozo, J. C., Wabnik, Krzysztof, Moreno-Risueño, Miguel Ángel, Ministerio de Economía y Competitividad (España), European Commission, Comunidad de Madrid, Research Foundation - Flanders, Agencia Estatal de Investigación (España), Ministerio de Ciencia e Innovación (España), Perianez-Rodriguez, Juan [0000-0003-1002-7111], Rodriguez, Marcos [0000-0003-3741-8593], Marconi, Marco [0000-0002-3457-1384], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Wachsman, Guy [0000-0002-0551-9333], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], De Gernier, Hugues [0000-0002-7644-3233], Cabrera, Javier [0000-0002-9277-4876], Perez-Garcia, Pablo [0000-0001-8595-8530], Gude, Inmaculada [0000-0002-3122-1688], Saez, Angela [0000-0002-9189-4737], Serrano-Ron, Laura [0000-0001-5180-6547], Beeckman, Tom [0000-0001-8656-2060], Benfey, Philip N [0000-0001-5302-758X], Rodríguez-Patón, Alfonso [0000-0001-7289-2114], del Pozo, J. C. [0000-0002-4113-457X], Wabnik, Krzysztof [0000-0001-7263-0560], Moreno-Risueno, Miguel A [0000-0002-9794-1450], Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, De Gernier, Hugues, Cabrera, Javier, Pérez-García, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N., Rodríguez-Patón, Alfonso, del Pozo, J. C., Wabnik, Krzysztof, and Moreno-Risueño, Miguel Ángel

Abstract

In Arabidopsis, the root clock regulates the spacing of lateral organs along the primary root through oscillating gene expression. The core molecular mechanism that drives the root clock periodicity and how it is modified by exogenous cues such as auxin and gravity remain unknown. We identified the key elements of the oscillator (AUXIN RESPONSE FACTOR 7, its auxin-sensitive inhibitor IAA18/POTENT, and auxin) that form a negative regulatory loop circuit in the oscillation zone. Through multilevel computer modeling fitted to experimental data, we explain how gene expression oscillations coordinate with cell division and growth to create the periodic pattern of organ spacing. Furthermore, gravistimulation experiments based on the model predictions show that external auxin stimuli can lead to entrainment of the root clock. Our work demonstrates the mechanism underlying a robust biological clock and how it can respond to external stimuli.

Published
2021

7. Fluorescence-Activated Cell Sorting Using the D-Root Device and Optimization for Scarce and/or Non-Accessible Root Cell Populations

Author

Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Comunidad de Madrid, González García, M. Paz [0000-0002-3739-3368], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], del Pozo, J. C. [0000-0002-4113-457X], Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], González García, M. Paz, Bustillo-Avendaño, Estefano, Sanchez-Corrionero, Alvaro, del Pozo, J. C., Moreno-Risueño, Miguel Ángel, Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Comunidad de Madrid, González García, M. Paz [0000-0002-3739-3368], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], del Pozo, J. C. [0000-0002-4113-457X], Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], González García, M. Paz, Bustillo-Avendaño, Estefano, Sanchez-Corrionero, Alvaro, del Pozo, J. C., and Moreno-Risueño, Miguel Ángel

Abstract

Fluorescence-activated cell sorting (FACS) is a technique used to isolate specific cell populations based on characteristics detected by flow cytometry. FACS has been broadly used in transcriptomic analyses of individual cell types during development or under different environmental conditions. Different protoplast extraction protocols are available for plant roots; however, they were designed for accessible cell populations, which normally were grown in the presence of light, a non-natural and stressful environment for roots. Here, we report a protocol using FACS to isolate root protoplasts from Arabidopsis green fluorescent protein (GFP)-marked lines using the minimum number of enzymes necessary for an optimal yield, and with the root system grown in darkness in the D-Root device. This device mimics natural conditions as the shoot grows in the presence of light while the roots grow in darkness. In addition, we optimized this protocol for specific patterns of scarce cell types inside more differentiated tissues using the mCherry fluorescent protein. We provide detailed experimental protocols for effective protoplasting, subsequent purification through FACS, and RNA extraction. Using this RNA, we generated cDNA and sequencing libraries, proving that our methods can be used for genome-wide transcriptomic analyses of any cell-type from roots grown in darkness.

Published
2020

9. An auxin-regulable oscillatory circuit drives the root clock in Arabidopsis

Author

Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, DeGernier, Hugues, Cabrera, Javier, Pérez-García, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N., Rodríguez-Patón, Alfonso, del Pozo, J. C., Wabnik, Krzysztof, Moreno-Risueño, Miguel Ángel, Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, DeGernier, Hugues, Cabrera, Javier, Pérez-García, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N., Rodríguez-Patón, Alfonso, del Pozo, J. C., Wabnik, Krzysztof, and Moreno-Risueño, Miguel Ángel

Abstract

In Arabidopsis, the root clock regulates the spacing of lateral organs along the primary root through oscillating gene expression. The core molecular mechanism that drives the root clock periodicity and how it is modified by exogenous cues such as auxin and gravity remain unknown. We identified the key elements of the oscillator (AUXIN RESPONSE FACTOR 7, its auxin-sensitive inhibitor IAA18/POTENT, and auxin) that form a negative regulatory loop circuit in the oscillation zone. Through multilevel computer modeling fitted to experimental data, we explain how gene expression oscillations coordinate with cell division and growth to create the periodic pattern of organ spacing. Furthermore, gravistimulation experiments based on the model predictions show that external auxin stimuli can lead to entrainment of the root clock. Our work demonstrates the mechanism underlying a robust biological clock and how it can respond to external stimuli.

Published
2021

10. Reconstruction of lateral root formation through single-cell RNA sequencing reveals order of tissue initiation

Author

European Commission, Universidad Politécnica de Madrid, Ministerio de Economía y Competitividad (España), Comunidad de Madrid, Agencia Estatal de Investigación (España), Serrano-Ron, L [0000-0001-5180-6547], Perez-Garcia, P [0000-0001-8595-8530], Sanchez-Corrionero, A [0000-0001-5360-0294], Gude, I [0000-0002-3122-1688], Cabrera, J [0000-0002-9277-4876], Birnbaum, KD [0000-0002-8423-6859], Moreno-Risueno, Miguel A [0000-0002-9794-1450], Serrano-Ron, Laura, Pérez-García, Pablo, Sanchez-Corrionero, Alvaro, Gude, Inmaculada, Cabrera, Javier, Ip, Pui-Leng, Birnbaum, KD, Moreno-Risueño, Miguel Ángel, European Commission, Universidad Politécnica de Madrid, Ministerio de Economía y Competitividad (España), Comunidad de Madrid, Agencia Estatal de Investigación (España), Serrano-Ron, L [0000-0001-5180-6547], Perez-Garcia, P [0000-0001-8595-8530], Sanchez-Corrionero, A [0000-0001-5360-0294], Gude, I [0000-0002-3122-1688], Cabrera, J [0000-0002-9277-4876], Birnbaum, KD [0000-0002-8423-6859], Moreno-Risueno, Miguel A [0000-0002-9794-1450], Serrano-Ron, Laura, Pérez-García, Pablo, Sanchez-Corrionero, Alvaro, Gude, Inmaculada, Cabrera, Javier, Ip, Pui-Leng, Birnbaum, KD, and Moreno-Risueño, Miguel Ángel

Abstract

Postembryonic organogenesis is critical for plant development. Underground, lateral roots (LRs) form the bulk of mature root systems, yet the ontogeny of the LR primordium (LRP) is not clear. In this study, we performed the single-cell RNA sequencing through the first four stages of LR formation in Arabidopsis. Our analysis led to a model in which a single group of precursor cells, with a cell identity different from their pericycle origins, rapidly reprograms and splits into a mixed ground tissue/stem cell niche fate and a vascular precursor fate. The ground tissue and stem cell niche fates soon separate and a subset of more specialized vascular cells form sucrose transporting phloem cells that appear to connect to the primary root. We did not detect cells resembling epidermis or root cap, suggesting that outer tissues may form later, preceding LR emergence. At this stage, some remaining initial precursor cells form the primordium flanks, while the rest create a reservoir of pluripotent cells that are able to replace the LR if damaged. Laser ablation of the central and lateral LRP regions showed that remaining cells restart the sequence of tissue initiation to form a LR. Collectively, our study reveals an ontological hierarchy for LR formation with an early and sequential split of main root tissues and stem cells.

Published
2021

11. An auxin-regulable oscillatory circuit drives the root clock in Arabidopsis

Author

Perianez-Rodriguez, Juan, primary, Rodriguez, Marcos, additional, Marconi, Marco, additional, Bustillo-Avendaño, Estefano, additional, Wachsman, Guy, additional, Sanchez-Corrionero, Alvaro, additional, De Gernier, Hugues, additional, Cabrera, Javier, additional, Perez-Garcia, Pablo, additional, Gude, Inmaculada, additional, Saez, Angela, additional, Serrano-Ron, Laura, additional, Beeckman, Tom, additional, Benfey, Philip N., additional, Rodríguez-Patón, Alfonso, additional, del Pozo, Juan Carlos, additional, Wabnik, Krzysztof, additional, and Moreno-Risueno, Miguel A., additional

Published
2021
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14. An auxin-regulable oscillatory circuit drives the root clock in Arabidopsis

Author

Marcos Rodriguez, Marco Marconi, Javier Cabrera, Miguel A. Moreno-Risueno, Laura Serrano-Ron, Angela Saez, Tom Beeckman, Philip N. Benfey, Juan Carlos del Pozo, Alfonso Rodríguez-Patón, Krzysztof Wabnik, Inmaculada Gude, Hugues De Gernier, Alvaro Sanchez-Corrionero, Juan Perianez-Rodriguez, Estefano Bustillo-Avendaño, Pablo Perez-Garcia, Guy Wachsman, Ministerio de Economía y Competitividad (España), European Commission, Comunidad de Madrid, Research Foundation - Flanders, Agencia Estatal de Investigación (España), Ministerio de Ciencia e Innovación (España), Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, De Gernier, Hugues, Cabrera, Javier, Perez-Garcia, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N, Rodríguez-Patón, Alfonso, Del Pozo, Juan Carlos, Wabnik, Krzysztof, Moreno-Risueno, Miguel A, Perianez-Rodriguez, Juan [0000-0003-1002-7111], Rodriguez, Marcos [0000-0003-3741-8593], Marconi, Marco [0000-0002-3457-1384], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Wachsman, Guy [0000-0002-0551-9333], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], De Gernier, Hugues [0000-0002-7644-3233], Cabrera, Javier [0000-0002-9277-4876], Perez-Garcia, Pablo [0000-0001-8595-8530], Gude, Inmaculada [0000-0002-3122-1688], Saez, Angela [0000-0002-9189-4737], Serrano-Ron, Laura [0000-0001-5180-6547], Beeckman, Tom [0000-0001-8656-2060], Benfey, Philip N [0000-0001-5302-758X], Rodríguez-Patón, Alfonso [0000-0001-7289-2114], Del Pozo, Juan Carlos [0000-0002-4113-457X], Wabnik, Krzysztof [0000-0001-7263-0560], and Moreno-Risueno, Miguel A [0000-0002-9794-1450]

Subjects
0106 biological sciences, Cell division, Digital storage, PROTEINS, Root (chord), CELL-DIVISION, 01 natural sciences, Plants (botany), 03 medical and health sciences, DOMAIN-II, Auxin, Arabidopsis, Timing circuits, LENGTH, TRAFFICKING, RNA-SEQ, Oscillating gene, Research Articles, Cell proliferation, 030304 developmental biology, GENE-EXPRESSION, chemistry.chemical_classification, Physics, 0303 health sciences, Multidisciplinary, biology, Oscillation, Plant Sciences, fungi, SciAdv r-articles, food and beverages, Biology and Life Sciences, Regulatory loop, DEGRADATION, biology.organism_classification, OF-FUNCTION MUTATION, chemistry, Biophysics, PATTERNS, Gene expression, Entrainment (chronobiology), 010606 plant biology & botany, Research Article
Abstract

CSIC - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), In Arabidopsis, the root clock regulates the spacing of lateral organs along the primary root through oscillating gene expression. The core molecular mechanism that drives the root clock periodicity and how it is modified by exogenous cues such as auxin and gravity remain unknown. We identified the key elements of the oscillator (AUXIN RESPONSE FACTOR 7, its auxin-sensitive inhibitor IAA18/POTENT, and auxin) that form a negative regulatory loop circuit in the oscillation zone. Through multilevel computer modeling fitted to experimental data, we explain how gene expression oscillations coordinate with cell division and growth to create the periodic pattern of organ spacing. Furthermore, gravistimulation experiments based on the model predictions show that external auxin stimuli can lead to entrainment of the root clock. Our work demonstrates the mechanism underlying a robust biological clock and how it can respond to external stimuli., This work was funded by the Ministerio de Economía y Competitividad of Spain (MINECO) and/or the ERDF (BFU2016-80315-P to M.A.M.-R., BIO2017-82209-R to J.C.d.P., and TIN2016-81079-R to A.R.-P.), the Comunidad de Madrid and/or ERDF and ESF (2017-T1/BIO-5654 to K.W. and S2017/BMD-3691 to A.R.-P.), the Howard Hughes Medical Institute and the NIH (R35-GM131725 to P.N.B.), the Fonds Wetenschappelijk Onderzoek (FWO Flanders) (G022516N, G020918N, and G024118N to T.B.), and the “Severo Ochoa Program for Centres of Excellence in R&D” from the Agencia Estatal de Investigacion of Spain [SEV-2016-0672 (2017–2021)] to K.W., P.P.-G., and M.A.M.-R. through CBGP. M.M. was supported by a postdoctoral contract associated to SEV-2016-0672, E.B.-A. by Ayudante de Investigacion contract PEJ-2017-AI/BIO-7360 from the Comunidad de Madrid, A.S.-C. and L.S.-R. by FPI contracts from MINECO (BES-2014-068852 and BES-2017-080155, respectively), J.C. by a Juan de la Cierva contract from MINECO (FJCI-2016-28607), P.P.-G. by a Juan de la Cierva contract from MINECO (FJCI-2015-24905) and Programa Atraccion Talento from Comunidad Madrid (2017-T2/BIO-3453), A.S. by a Torres Quevedo contract from MINECO (PTQ-15-07915), and K.W. by program PGC2018-093387-A-I00 from the Ministerio de Ciencia e Innovacion (MICIU)

Published
2021

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